Evolution in arid environments: the role of betalains, succulence, and medullary bundles

The flowering plant clade Caryophyllales includes many succulent species that grow in drought conditions. Many Caryophyllales species also have betalain pigmentation and medullary bundles, both of which have been linked to stress tolerance, albeit with less precise functional characterisation. We investigated the relationship between the evolution of these traits and drought tolerance in Caryophyllales. We estimated divergence times for Caryophyllales using transcriptomic data; a 50-character morphological matrix based on a comprehensive review of Caryophyllales fossils; a species-level molecular dataset incorporating >4,400 species; and a tip-dating approach. This enabled us to analyse the evolution of drought tolerance, succulence, betalain pigmentation, and medullary bundles. We demonstrate that betalain-pigmented lineages primarily experience drought conditions, with betalains appearing to evolve repeatedly in response to drought during the early evolution of Caryophyllales. We also show that the evolution of succulence and medullary bundles is favoured in betalain-pigmented lineages. However, medullary bundles, unlike succulence, do not show a clear relationship with drought conditions. The evolution of betalains is likely enabled Caryophyllales to adapt to and survive stressful conditions, including drought. This may have increased the adaptive advantages of succulence, as its extensive costs are likely offset by its benefits in drought conditions.